Population viscosity can promote the evolution of altruistic sterile helpers and eusociality

Because it increases relatedness between interacting individuals, population viscosity has been proposed to favour the evolution of altruistic helping. However, because it increases local competition between relatives, population viscosity may also act as a brake for the evolution of helping behaviours. In simple models, the kin selected fecundity benefits of helping are exactly cancelled out by the cost of increased competition between relatives when helping occurs after dispersal. This result has lead to the widespread view, especially among people working with social organisms, that special conditions are required for the evolution of altruism. Here, we re-examine this result by constructing a simple population genetic model where we analyse whether the evolution of a sterile worker caste (i.e. an extreme case of altruism) can be selected for by limited dispersal. We show that a sterile worker caste can be selected for even under the simplest life-cycle assumptions. This has relevant consequences for our understanding of the evolution of altruism in social organisms, as many social insects are characterized by limited dispersal and significant genetic population structure.

[1]  Kenichi Aoki,et al.  A CONDITION FOR GROUP SELECTION TO PREVAIL OVER COUNTERACTING INDIVIDUAL SELECTION , 1982, Evolution; international journal of organic evolution.

[2]  I. Eshel On the neighbor effect and the evolution of altruistic traits. , 1972, Theoretical population biology.

[3]  A. Gardner,et al.  Demography, altruism, and the benefits of budding , 2006, Journal of evolutionary biology.

[4]  W. Hamilton,et al.  Selfish and Spiteful Behaviour in an Evolutionary Model , 1970, Nature.

[5]  A. Griffin,et al.  Cooperation and Competition Between Relatives , 2002, Science.

[6]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[7]  F. Balloux,et al.  The estimation of population differentiation with microsatellite markers , 2002, Molecular ecology.

[8]  Andy Gardner,et al.  Cooperation and the Scale of Competition in Humans , 2006, Current Biology.

[9]  L. Keller,et al.  Assessing genetic structure with multiple classes of molecular markers: a case study involving the introduced fire ant Solenopsis invicta. , 1999, Molecular biology and evolution.

[10]  T. Burke,et al.  Isolation by distance and gene flow in the Eurasian badger (Meles meles) at both a local and broad scale , 2005, Molecular ecology.

[11]  P D Taylor,et al.  Evolution of altruism in stepping-stone populations with overlapping generations. , 2001, Theoretical population biology.

[12]  S. Aron,et al.  Inbreeding and kinship in the ant Plagiolepis pygmaea , 2005, Molecular ecology.

[13]  L. Keller,et al.  Social life: the paradox of multiple-queen colonies. , 1995, Trends in ecology & evolution.

[14]  T. Nagylaki The robustness of neutral models of geographical variation , 1983 .

[15]  J. S. Pedersen,et al.  Effect of habitat saturation on the number and turnover of queens in the polygynous ant, Myrmica sulcinodis , 1999 .

[16]  D. Queller,et al.  Does population viscosity promote kin selection? , 1992, Trends in ecology & evolution.

[17]  Astrid Hopfensitz,et al.  In love and war: altruism, norm formation, and two different types of group selection. , 2007, Journal of theoretical biology.

[18]  A Grafen,et al.  An inclusive fitness analysis of altruism on a cyclical network , 2007, Journal of evolutionary biology.

[19]  V. Jansen,et al.  Altruism through beard chromodynamics , 2006, Nature.

[20]  J. Herbers,et al.  Population structure of Leptothorax ambiguus, a facultatively polygynous and polydomous ant species , 1994 .

[21]  L. Sundström Genetic population structure and sociogenetic organisation in Formica truncorum (Hymenoptera; Formicidae) , 1993, Behavioral Ecology and Sociobiology.

[22]  Joe Yuichiro Wakano,et al.  Evolution of cooperation in spatial public goods games with common resource dynamics. , 2007, Journal of theoretical biology.

[23]  P. Pamilo GENETIC DIFFERENTIATION WITHIN SUBDIVIDED POPULATIONS OF FORMICA ANTS , 1983, Evolution; international journal of organic evolution.

[24]  G Malécot,et al.  Heterozygosity and relationship in regularly subdivided populations. , 1975, Theoretical population biology.

[25]  P. Taylor An inclusive fitness model for dispersal of offspring , 1988 .

[26]  H. Gintis,et al.  The evolution of strong reciprocity: cooperation in heterogeneous populations. , 2004, Theoretical population biology.

[27]  L. Keller,et al.  MICROSATELLITES REVEAL HIGH POPULATION VISCOSITY AND LIMITED DISPERSAL IN THE ANT FORMICA PARALUGUBRIS , 1997, Evolution; international journal of organic evolution.

[28]  M. Baalen,et al.  Self-structuring in spatial evolutionary ecology. , 2008, Ecology letters.

[29]  D. Sumpter,et al.  The evolution of helping and harming on graphs: the return of the inclusive fitness effect , 2007, Journal of evolutionary biology.

[30]  N. Franks,et al.  Social Evolution in Ants , 2019 .

[31]  F. Rousset,et al.  CONSTRAINTS ON THE ORIGIN AND MAINTENANCE OF GENETIC KIN RECOGNITION , 2007, Evolution; international journal of organic evolution.

[32]  T Nagylaki The decay of genetic variability in geographically structured populations. II. , 1976, Theoretical population biology.

[33]  T. Nagylaki The decay of genetic variability in geographically structured populations. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[34]  H. Ohtsuki,et al.  A simple rule for the evolution of cooperation on graphs and social networks , 2006, Nature.

[35]  P. Taylor Altruism in viscous populations — an inclusive fitness model , 1992, Evolutionary Ecology.

[36]  Laurent Lehmann,et al.  THE ADAPTIVE DYNAMICS OF NICHE CONSTRUCTING TRAITS IN SPATIALLY SUBDIVIDED POPULATIONS: EVOLVING POSTHUMOUS EXTENDED PHENOTYPES , 2008, Evolution; international journal of organic evolution.

[37]  T. Maruyama,et al.  Effective number of alleles in a subdivided population. , 1970, Theoretical population biology.

[38]  M. Baalen,et al.  The Unit of Selection in Viscous Populations and the Evolution of Altruism. , 1998, Journal of theoretical biology.

[39]  Alan Grafen,et al.  Detecting kin selection at work using inclusive fitness , 2007, Proceedings of the Royal Society B: Biological Sciences.

[40]  Alan R. Rogers,et al.  Group Selection by Selective Emigration: The Effects of Migration and Kin Structure , 1990, The American Naturalist.

[41]  F. Rousset,et al.  Evolution of stepping-stone dispersal rates , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  M. Higashi,et al.  Evolution of mutualism through spatial effects. , 2004, Journal of theoretical biology.

[43]  U. Dieckmann,et al.  THE ADAPTIVE DYNAMICS OF ALTRUISM IN SPATIALLY HETEROGENEOUS POPULATIONS , 2003, Evolution; international journal of organic evolution.

[44]  F. Rousset,et al.  POPULATION DEMOGRAPHY AND THE EVOLUTION OF HELPING BEHAVIORS , 2006, Evolution; international journal of organic evolution.

[45]  T. Nagylaki,et al.  Decay of genetic variability in geographically structured populations. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[46]  B. Epperson Gene genealogies in geographically structured populations. , 1999, Genetics.

[47]  F. Rousset Genetic Structure and Selection in Subdivided Populations (MPB-40) , 2004 .

[48]  Peter D. Taylor,et al.  Inclusive fitness in a homogeneous environment , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  S. Frank Foundations of Social Evolution , 2019 .

[50]  L. Keller,et al.  Hierarchical analysis of genetic structure in native fire ant populations: results from three classes of molecular markers. , 1997, Genetics.

[51]  Tom Wenseleers,et al.  Altruism in insect societies and beyond: voluntary or enforced? , 2008, Trends in ecology & evolution.

[52]  D. E. Matthews Evolution and the Theory of Games , 1977 .

[53]  P. Taylor,et al.  How to make a kin selection model. , 1996, Journal of theoretical biology.

[54]  Rousset,et al.  A theoretical basis for measures of kin selection in subdivided populations: finite populations and localized dispersal , 2000 .

[55]  D. Wilson,et al.  Population viscosity and the evolution of altruism. , 2000, Journal of theoretical biology.

[56]  Peter D. Taylor,et al.  Allele-Frequency Change in a Class-Structured Population , 1990, The American Naturalist.

[57]  N. Perrin,et al.  Local Competition, Inbreeding, and the Evolution of Sex‐Biased Dispersal , 2000, The American Naturalist.

[58]  P D Taylor,et al.  OVERLAPPING GENERATIONS CAN PROMOTE ALTRUISTIC BEHAVIOR , 2000, Evolution; international journal of organic evolution.